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Published in: Neurological Sciences 10/2020

01-10-2020 | Coronavirus | COVID-19

Neuroinvasion, neurotropic, and neuroinflammatory events of SARS-CoV-2: understanding the neurological manifestations in COVID-19 patients

Authors: Yassine Yachou, Abdeslem El Idrissi, Vladimir Belapasov, Said Ait Benali

Published in: Neurological Sciences | Issue 10/2020

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Abstract

Respiratory viruses are opportunistic pathogens that infect the upper respiratory tract in humans and cause severe illnesses, especially in vulnerable populations. Some viruses have neuroinvasive properties and activate the immune response in the brain. These immune events may be neuroprotective or they may cause long-term damage similar to what is seen in some neurodegenerative diseases. The new “Severe Acute Respiratory Syndrome Coronavirus 2” (SARS-CoV-2) is one of the Respiratory viruses causing highly acute lethal pneumonia coronavirus disease 2019 (COVID-19) with clinical similarities to those reported in “Severe Acute Respiratory Syndrome Coronavirus”(SARS-CoV) and the “Middle East Respiratory Syndrome Coronavirus”(MERS-CoV) including neurological manifestation. To examine the possible neurological damage induced by SARS-CoV-2, it is necessary to understand the immune reactions to viral infection in the brain, and their short- and long-term consequences. Considering the similarities between SARS-CoV and SARS-CoV-2, which will be discussed, cooperative homological and phylogenetical studies lead us to question if SARS-CoV-2 can have similar neuroinvasive capacities and neuroinflammatiory events that may lead to the same short- and long-term neuropathologies that SARS-CoV had shown in human and animal models. To explain the neurological manifestation caused by SARS-CoV-2, we will present a literature review of 765 COVID-19 patients, in which 18% had neurological symptoms and complications, including encephalopathy, encephalitis and cerebrovascular pathologies, acute myelitis, and Guillain-Barré syndrome. Clinical studies describe anosmia or partial loss of the sense of smell as the most frequent symptom in COVID19 patients, suggesting that olfactory dysfunction and the initial ultrarapid immune responses could be a prognostic factor.
Literature
6.
go back to reference Streit WJ (2006) Microglial senescence: does the brain’s immune system have an expiration date? Trends Neurosci 29:506–510PubMed Streit WJ (2006) Microglial senescence: does the brain’s immune system have an expiration date? Trends Neurosci 29:506–510PubMed
7.
go back to reference Streit WJ, Mrak RE, Griffin WS (2004) Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 1:14PubMedPubMedCentral Streit WJ, Mrak RE, Griffin WS (2004) Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation 1:14PubMedPubMedCentral
8.
go back to reference von Bernhardi R (2007) Glial cell dysregulation: a new perspective on Alzheimer Disease. Neurotox Res 12:215–232 von Bernhardi R (2007) Glial cell dysregulation: a new perspective on Alzheimer Disease. Neurotox Res 12:215–232
9.
go back to reference Nakajima K, Tohyama Y, Kohsaka S, Kurihara T (2001) Ability of rat microglia to uptake extracellular glutamate. Neurosci Lett 307:171–174PubMed Nakajima K, Tohyama Y, Kohsaka S, Kurihara T (2001) Ability of rat microglia to uptake extracellular glutamate. Neurosci Lett 307:171–174PubMed
10.
go back to reference van den Pol AN (2006) Viral infections in the developing and mature brain. Trends Neurosci 29:398–406PubMed van den Pol AN (2006) Viral infections in the developing and mature brain. Trends Neurosci 29:398–406PubMed
11.
go back to reference Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA (2004) Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10:1366–1373PubMed Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA (2004) Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10:1366–1373PubMed
12.
go back to reference Boulanger LM (2009) Immune proteins in brain development and synaptic plasticity. Neuron. 64:93–109PubMed Boulanger LM (2009) Immune proteins in brain development and synaptic plasticity. Neuron. 64:93–109PubMed
13.
go back to reference Deleidi M, Hallett PJ, Koprich JB, Chung CY, Isacson O (2010) The Toll-like receptor-3 agonist polyinosinic:polycytidylic acid triggers nigrostriatal dopaminergic degeneration. J Neurosci 30:16091–16101PubMedPubMedCentral Deleidi M, Hallett PJ, Koprich JB, Chung CY, Isacson O (2010) The Toll-like receptor-3 agonist polyinosinic:polycytidylic acid triggers nigrostriatal dopaminergic degeneration. J Neurosci 30:16091–16101PubMedPubMedCentral
14.
go back to reference Chung CY, Koprich JB, Siddiqi H, Isacson O (2009) Dynamic changes in presynaptic and axonal transport proteins combined with striatal neuroinflammation precede dopaminergic neuronal loss in a rat model of AAV alpha-synucleinopathy. J Neurosci 29:3365–3373PubMedPubMedCentral Chung CY, Koprich JB, Siddiqi H, Isacson O (2009) Dynamic changes in presynaptic and axonal transport proteins combined with striatal neuroinflammation precede dopaminergic neuronal loss in a rat model of AAV alpha-synucleinopathy. J Neurosci 29:3365–3373PubMedPubMedCentral
15.
go back to reference Centonze D, Muzio L, Rossi S, Cavasinni F, De Chiara V, Bergami A, Musella A, D’Amelio M, Cavallucci V, Martorana A, Bergamaschi A, Cencioni MT, Diamantini A, Butti E, Comi G, Bernardi G, Cecconi F, Battistini L, Furlan R, Martino G (2009) Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J Neurosci 29:3442–3452PubMedPubMedCentral Centonze D, Muzio L, Rossi S, Cavasinni F, De Chiara V, Bergami A, Musella A, D’Amelio M, Cavallucci V, Martorana A, Bergamaschi A, Cencioni MT, Diamantini A, Butti E, Comi G, Bernardi G, Cecconi F, Battistini L, Furlan R, Martino G (2009) Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J Neurosci 29:3442–3452PubMedPubMedCentral
16.
go back to reference Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572–580PubMed Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572–580PubMed
17.
go back to reference Arkwright PD, Abinun M (2008) Recently identified factors predisposing children to infectious diseases. Curr Opin Infect Dis 21:217–222PubMed Arkwright PD, Abinun M (2008) Recently identified factors predisposing children to infectious diseases. Curr Opin Infect Dis 21:217–222PubMed
18.
go back to reference Bohmwald K, Espinoza JA, Gonzalez PA, Bueno SM, Riedel CA, Kalergis AM (2014) Central nervous system alterations caused by infection with the human respiratory syncytial virus. Rev Med Virol 24:407–419PubMed Bohmwald K, Espinoza JA, Gonzalez PA, Bueno SM, Riedel CA, Kalergis AM (2014) Central nervous system alterations caused by infection with the human respiratory syncytial virus. Rev Med Virol 24:407–419PubMed
19.
go back to reference Halfhide CP, Flanagan BF, Brearey SP, Hunt JA, Fonceca AM, McNamara PS, Howarth D, Edwards S, Smyth RL (2011) Respiratory syncytial virus binds and undergoes transcription in neutrophils from the blood and airways of infants with severe bronchiolitis. J Infect Dis 204:451–458PubMedPubMedCentral Halfhide CP, Flanagan BF, Brearey SP, Hunt JA, Fonceca AM, McNamara PS, Howarth D, Edwards S, Smyth RL (2011) Respiratory syncytial virus binds and undergoes transcription in neutrophils from the blood and airways of infants with severe bronchiolitis. J Infect Dis 204:451–458PubMedPubMedCentral
20.
go back to reference Mathieu C, Pohl C, Szecsi J, Trajkovic-Bodennec S, Devergnas S, Raoul H, Cosset FL, Gerlier D, Wild TF, Horvat B (2011) Nipah virus usesleukocytes for efficient dissemination within a host. J Virol 85:7863–7871 Mathieu C, Pohl C, Szecsi J, Trajkovic-Bodennec S, Devergnas S, Raoul H, Cosset FL, Gerlier D, Wild TF, Horvat B (2011) Nipah virus usesleukocytes for efficient dissemination within a host. J Virol 85:7863–7871
21.
go back to reference Escaffre O, Borisevich V, Carmical JR, Prusak D, Prescott J, Feldmann H, Rockx B (2013) Henipavirus pathogenesis in human respiratory epithelial cells. J Virol 87:3284–3294PubMedPubMedCentral Escaffre O, Borisevich V, Carmical JR, Prusak D, Prescott J, Feldmann H, Rockx B (2013) Henipavirus pathogenesis in human respiratory epithelial cells. J Virol 87:3284–3294PubMedPubMedCentral
22.
go back to reference Tse H, To KK, Wen X, Chen H, Chan KH, Tsoi HW, Li IW, Yuen KY (2011) Clinical and virological factors associated with viremia in pandemic influenza A/H1N1/2009 virus infection. PLoS One 6:e22534PubMedPubMedCentral Tse H, To KK, Wen X, Chen H, Chan KH, Tsoi HW, Li IW, Yuen KY (2011) Clinical and virological factors associated with viremia in pandemic influenza A/H1N1/2009 virus infection. PLoS One 6:e22534PubMedPubMedCentral
23.
go back to reference Imamura T, Suzuki A, Lupisan S, Kamigaki T, Okamoto M, Roy CN, Olveda R, Oshitani H (2014) Detection of enterovirus 68 in serum from pediatric patients with pneumonia and their clinical outcomes. Influenza Other Respir Viruses 8:21–24PubMed Imamura T, Suzuki A, Lupisan S, Kamigaki T, Okamoto M, Roy CN, Olveda R, Oshitani H (2014) Detection of enterovirus 68 in serum from pediatric patients with pneumonia and their clinical outcomes. Influenza Other Respir Viruses 8:21–24PubMed
24.
go back to reference Berth SH, Leopold PL, Morfini GN (2009) Virus-induced neuronal dysfunction and degeneration. Front Biosci 14:5239–5259 Berth SH, Leopold PL, Morfini GN (2009) Virus-induced neuronal dysfunction and degeneration. Front Biosci 14:5239–5259
25.
go back to reference Mori I (2015) Transolfactory neuroinvasion by viruses threatens the human brain. Acta Virol 59:338–349PubMed Mori I (2015) Transolfactory neuroinvasion by viruses threatens the human brain. Acta Virol 59:338–349PubMed
26.
go back to reference Lochhead JJ, Thorne RG (2012) Intranasal delivery of biologics to the central nervous system. Adv Drug Deliv Rev 64:614–628PubMed Lochhead JJ, Thorne RG (2012) Intranasal delivery of biologics to the central nervous system. Adv Drug Deliv Rev 64:614–628PubMed
27.
go back to reference Lochhead JJ, Kellohen KL, Ronaldson PT, Davis TP (2019) Distribution of insulin in trigeminal nerve and brain after intranasal administration. Sci Rep 9:2621PubMedPubMedCentral Lochhead JJ, Kellohen KL, Ronaldson PT, Davis TP (2019) Distribution of insulin in trigeminal nerve and brain after intranasal administration. Sci Rep 9:2621PubMedPubMedCentral
28.
go back to reference Driessen AK, Farrell MJ, Mazzone SB, McGovern AE (2016) Multiple neural circuits mediating airway sensations: recent advances in the neurobiology of the urge-to-cough. Respir Physiol Neurobiol 226:115–120PubMed Driessen AK, Farrell MJ, Mazzone SB, McGovern AE (2016) Multiple neural circuits mediating airway sensations: recent advances in the neurobiology of the urge-to-cough. Respir Physiol Neurobiol 226:115–120PubMed
29.
go back to reference Goenka A, Michael BD, Ledger E, Hart IJ, Absoud M, Chow G, Lilleker J, Lunn M, McKee D, Peake D, Pysden K, Roberts M, Carrol ED, Lim M, Avula S, Solomon T, Kneen R (2014) Neurological manifestations of influenza infection in children and adults: results of a national british surveillance study. Clin Infect Dis 58:775–784. https://doi.org/10.1093/cid/cit922CrossRefPubMed Goenka A, Michael BD, Ledger E, Hart IJ, Absoud M, Chow G, Lilleker J, Lunn M, McKee D, Peake D, Pysden K, Roberts M, Carrol ED, Lim M, Avula S, Solomon T, Kneen R (2014) Neurological manifestations of influenza infection in children and adults: results of a national british surveillance study. Clin Infect Dis 58:775–784. https://​doi.​org/​10.​1093/​cid/​cit922CrossRefPubMed
30.
34.
go back to reference Sivadon-Tardy V, Orlikowski D, Porcher R, Sharshar T, Durand MC, Enouf V, Rozenberg F, Caudie C, Annane D, van der Werf S, Lebon P, Raphaël JC, Gaillard JL, Gault E (2009) Guillain-Barré syndrome and influenza virus infection. Clin Infect Dis 48(1):48–56. https://doi.org/10.1086/594124CrossRefPubMed Sivadon-Tardy V, Orlikowski D, Porcher R, Sharshar T, Durand MC, Enouf V, Rozenberg F, Caudie C, Annane D, van der Werf S, Lebon P, Raphaël JC, Gaillard JL, Gault E (2009) Guillain-Barré syndrome and influenza virus infection. Clin Infect Dis 48(1):48–56. https://​doi.​org/​10.​1086/​594124CrossRefPubMed
36.
go back to reference Zeng H, Quinet S, Huang W, Gan Y, Han C, He Y, Wang Y (2013) Clinical and MRI features of neurological complications after influenza A (H1N1) infection in critically ill children. Pediatr Radiol 43:1182–1189PubMed Zeng H, Quinet S, Huang W, Gan Y, Han C, He Y, Wang Y (2013) Clinical and MRI features of neurological complications after influenza A (H1N1) infection in critically ill children. Pediatr Radiol 43:1182–1189PubMed
37.
go back to reference Beraki S, Aronsson F, Karlsson H, Ogren SO, Kristensson K (2005) Influenza a virus infection causes alterations in expression of synaptic regulatory genes combined with changes in cognitive and emotional behaviors in mice. Mol Psychiatry 10:299–308PubMed Beraki S, Aronsson F, Karlsson H, Ogren SO, Kristensson K (2005) Influenza a virus infection causes alterations in expression of synaptic regulatory genes combined with changes in cognitive and emotional behaviors in mice. Mol Psychiatry 10:299–308PubMed
38.
go back to reference Hosseini S, Wilk E, Michaelsen-Preusse K, Gerhauser I, Baumgartner W, Geffers R, Schughart K, Korte M (2018) Long-term neuroinflammation induced by influenza a virus infection and the impact on hippocampal neuron morphology and function. J Neurosci 38:3060–3080PubMedPubMedCentral Hosseini S, Wilk E, Michaelsen-Preusse K, Gerhauser I, Baumgartner W, Geffers R, Schughart K, Korte M (2018) Long-term neuroinflammation induced by influenza a virus infection and the impact on hippocampal neuron morphology and function. J Neurosci 38:3060–3080PubMedPubMedCentral
39.
go back to reference Matsuda K, Park CH, Sunden Y, Kimura T, Ochiai K, Kida H, Umemura T (2004) The vagus nerve is one route of transneural invasion for intranasally inoculated influenza a virus in mice. Vet Pathol 41:101–107PubMed Matsuda K, Park CH, Sunden Y, Kimura T, Ochiai K, Kida H, Umemura T (2004) The vagus nerve is one route of transneural invasion for intranasally inoculated influenza a virus in mice. Vet Pathol 41:101–107PubMed
40.
go back to reference Shinya K, Makino A, Hatta M, Watanabe S, Kim JH, Hatta Y, Gao P, Ozawa M, Le QM, Kawaoka Y (2011) Subclinical brain injury caused by H5N1 influenza virus infection. J Virol 85:5202–5207PubMedPubMedCentral Shinya K, Makino A, Hatta M, Watanabe S, Kim JH, Hatta Y, Gao P, Ozawa M, Le QM, Kawaoka Y (2011) Subclinical brain injury caused by H5N1 influenza virus infection. J Virol 85:5202–5207PubMedPubMedCentral
41.
go back to reference Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, Smeyne RJ (2009) Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci U S A 106:14063–14068PubMedPubMedCentral Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, Smeyne RJ (2009) Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci U S A 106:14063–14068PubMedPubMedCentral
42.
go back to reference King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (Eds) (2012) Classification and nomenclature of viruses. In: Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier: San Diego, 1326–1327 King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (Eds) (2012) Classification and nomenclature of viruses. In: Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier: San Diego, 1326–1327
43.
go back to reference Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, Tong S, Urbani C, Comer JA, Lim W, Rollin PE, Dowell SF, Ling AE, Humphrey CD, Shieh WJ, Guarner J, Paddock CD, Rota P, Fields B, DeRisi J, Yang JY, Cox N, Hughes JM, LeDuc J, Bellini WJ, Anderson LJ, SARS Working Group (2003) A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 348:1953–1966PubMed Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, Tong S, Urbani C, Comer JA, Lim W, Rollin PE, Dowell SF, Ling AE, Humphrey CD, Shieh WJ, Guarner J, Paddock CD, Rota P, Fields B, DeRisi J, Yang JY, Cox N, Hughes JM, LeDuc J, Bellini WJ, Anderson LJ, SARS Working Group (2003) A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med 348:1953–1966PubMed
44.
go back to reference Sheahan TP, Sims AC, Leist SR, Schäfer A, Won J, Brown AJ, Montgomery SA, Hogg A, Babusis D, Clarke MO, Spahn JE, Bauer L, Sellers S, Porter D, Feng JY, Cihlar T, Jordan R, Denison MR, Baric RS (2020) Comparative therapeutic efficacy of remdesivir and combination lopinavir, ritonavir, and interferon beta against MERS-CoV. Nat Commun 11:222PubMedPubMedCentral Sheahan TP, Sims AC, Leist SR, Schäfer A, Won J, Brown AJ, Montgomery SA, Hogg A, Babusis D, Clarke MO, Spahn JE, Bauer L, Sellers S, Porter D, Feng JY, Cihlar T, Jordan R, Denison MR, Baric RS (2020) Comparative therapeutic efficacy of remdesivir and combination lopinavir, ritonavir, and interferon beta against MERS-CoV. Nat Commun 11:222PubMedPubMedCentral
45.
go back to reference de Groot RJ, Baker SC, Baric RS et al (2013) Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group. J Virol 87:7790–7792PubMedPubMedCentral de Groot RJ, Baker SC, Baric RS et al (2013) Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group. J Virol 87:7790–7792PubMedPubMedCentral
46.
go back to reference Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus ADME, Fouchier RAM (2012) Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367:1814–1820PubMed Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus ADME, Fouchier RAM (2012) Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med 367:1814–1820PubMed
48.
go back to reference Gerna G, Passarani N, Battaglia M, Rondanelli EG (1985) Human enteric coronaviruses: antigenic relatedness to human coronavirus OC43 and possible etiologic role in viral gastroenteritis. J Infect Dis 151:796–803PubMedPubMedCentral Gerna G, Passarani N, Battaglia M, Rondanelli EG (1985) Human enteric coronaviruses: antigenic relatedness to human coronavirus OC43 and possible etiologic role in viral gastroenteritis. J Infect Dis 151:796–803PubMedPubMedCentral
49.
go back to reference Jevsnik M, Steyer A, Pokorn M, Mrvic T, Grosek S, Strle F, Lusa L, Petrovec M (2016) The role of human coronaviruses in children hospitalized for acute bronchiolitis, acute gastroenteritis, and febrile seizures: a 2-year prospective study. PLoS One 11:e0155555PubMedPubMedCentral Jevsnik M, Steyer A, Pokorn M, Mrvic T, Grosek S, Strle F, Lusa L, Petrovec M (2016) The role of human coronaviruses in children hospitalized for acute bronchiolitis, acute gastroenteritis, and febrile seizures: a 2-year prospective study. PLoS One 11:e0155555PubMedPubMedCentral
50.
go back to reference Raj VS, Osterhaus AD, Fouchier RA, Haagmans BL (2014) MERS: emergence of a novel human coronavirus. Curr Opin Virol 5:58–62PubMedPubMedCentral Raj VS, Osterhaus AD, Fouchier RA, Haagmans BL (2014) MERS: emergence of a novel human coronavirus. Curr Opin Virol 5:58–62PubMedPubMedCentral
51.
go back to reference Resta S, Luby JP, Rosenfeld CR, Siegel JD (1985) Isolation and propagation of a human enteric coronavirus. Science 229:978–981PubMed Resta S, Luby JP, Rosenfeld CR, Siegel JD (1985) Isolation and propagation of a human enteric coronavirus. Science 229:978–981PubMed
52.
go back to reference Riski H, Hovi T (1980) Coronavirus infections of man associated with diseases other than the common cold. J Med Virol 6:259–265PubMedPubMedCentral Riski H, Hovi T (1980) Coronavirus infections of man associated with diseases other than the common cold. J Med Virol 6:259–265PubMedPubMedCentral
53.
go back to reference Jiang G, Gong E, Zhang B, Zheng J, Gao Z, Zhong Y, Zou W, Zhan J, Wang S, Xie Z, Zhuang H, Wu B, Zhong H, Shao H, Fang W, Gao D, Pei F, Li X, He Z, Xu D, Shi X, Anderson VM, Leong AS-Y (2005) Multiple organ infection and the pathogenesis of SARS. J Exp Med 202(3):415–424 Jiang G, Gong E, Zhang B, Zheng J, Gao Z, Zhong Y, Zou W, Zhan J, Wang S, Xie Z, Zhuang H, Wu B, Zhong H, Shao H, Fang W, Gao D, Pei F, Li X, He Z, Xu D, Shi X, Anderson VM, Leong AS-Y (2005) Multiple organ infection and the pathogenesis of SARS. J Exp Med 202(3):415–424
58.
go back to reference Desforges M, Le Coupanec A, Brison É, Meessen-Pinard M, Talbot PJ (2014) Neuroinvasive and neurotropic human respiratory coronaviruses: potential neurovirulent agents in humans. In: Adhikari R, Thapa S (eds) Infectious Diseases and Nanomedicine I. Springer, India, pp 75–96 Desforges M, Le Coupanec A, Brison É, Meessen-Pinard M, Talbot PJ (2014) Neuroinvasive and neurotropic human respiratory coronaviruses: potential neurovirulent agents in humans. In: Adhikari R, Thapa S (eds) Infectious Diseases and Nanomedicine I. Springer, India, pp 75–96
62.
go back to reference Li Z, He W, Lan Y, Zhao K, Lv X, Lu H, Ding N, Zhang J, Shi J, Shan C, Gao F (2016) The evidence of porcine hemagglutinating encephalomyelitis virus induced nonsuppurative encephalitis as the cause of death in piglets. Peer J 4:e2443PubMed Li Z, He W, Lan Y, Zhao K, Lv X, Lu H, Ding N, Zhang J, Shi J, Shan C, Gao F (2016) The evidence of porcine hemagglutinating encephalomyelitis virus induced nonsuppurative encephalitis as the cause of death in piglets. Peer J 4:e2443PubMed
63.
go back to reference Chen C, Zhang XR, Ju ZY, He WF (2020) Advances in the research of cytokine storm mechanism induced by Corona Virus Disease 2019 and the corresponding immunotherapies. Zhonghua Shao Shang Za Zhi 36:E005 Chen C, Zhang XR, Ju ZY, He WF (2020) Advances in the research of cytokine storm mechanism induced by Corona Virus Disease 2019 and the corresponding immunotherapies. Zhonghua Shao Shang Za Zhi 36:E005
64.
go back to reference Mengeling WL, Boothe AD, Ritchie AE (1972) Characteristics of a coronavirus (strain 67N) of pigs. Am J Vet Res 33(2):297–308 Mengeling WL, Boothe AD, Ritchie AE (1972) Characteristics of a coronavirus (strain 67N) of pigs. Am J Vet Res 33(2):297–308
65.
go back to reference Andries K, Pensaert MB (1980) Virus isolated and immunofluorescence in different organs of pigs infected with hemagglutinating encephalomyelitis virus. Am J Vet Res 41:215–218 Andries K, Pensaert MB (1980) Virus isolated and immunofluorescence in different organs of pigs infected with hemagglutinating encephalomyelitis virus. Am J Vet Res 41:215–218
68.
go back to reference Lu R, Zhao X, Li J, Niu P, Yang B, Wu H, Wang W, Song H, Huang B, Zhu N, Bi Y, Ma X, Zhan F, Wang L, Hu T, Zhou H, Hu Z, Zhou W, Zhao L, Chen J, Meng Y, Wang J, Lin Y, Yuan J, Xie Z, Ma J, Liu WJ, Wang D, Xu W, Holmes EC, Gao GF, Wu G, Chen W, Shi W, Tan W (2020) Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet. 395(10224):565–574. https://doi.org/10.1016/S0140-6736(20)30251-8CrossRefPubMedPubMedCentral Lu R, Zhao X, Li J, Niu P, Yang B, Wu H, Wang W, Song H, Huang B, Zhu N, Bi Y, Ma X, Zhan F, Wang L, Hu T, Zhou H, Hu Z, Zhou W, Zhao L, Chen J, Meng Y, Wang J, Lin Y, Yuan J, Xie Z, Ma J, Liu WJ, Wang D, Xu W, Holmes EC, Gao GF, Wu G, Chen W, Shi W, Tan W (2020) Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet. 395(10224):565–574. https://​doi.​org/​10.​1016/​S0140-6736(20)30251-8CrossRefPubMedPubMedCentral
69.
go back to reference Tsai LK, Hsieh ST, Chang YC (2005) Neurological manifestations in severe acute respiratory syndrome. Acta Neurol Taiwanica 14(3):113–119 Tsai LK, Hsieh ST, Chang YC (2005) Neurological manifestations in severe acute respiratory syndrome. Acta Neurol Taiwanica 14(3):113–119
71.
go back to reference McCray PB Jr, Pewe L, Wohlford-Lenane C, Hickey M, Manzel L, Shi L, Netland J, Jia HP, Halabi C, Sigmund CD, Meyerholz DK, Kirby P, Look DC, Perlman S (2007) Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J Virol 81(2):813–821. https://doi.org/10.1128/JVI.02012-06CrossRefPubMed McCray PB Jr, Pewe L, Wohlford-Lenane C, Hickey M, Manzel L, Shi L, Netland J, Jia HP, Halabi C, Sigmund CD, Meyerholz DK, Kirby P, Look DC, Perlman S (2007) Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J Virol 81(2):813–821. https://​doi.​org/​10.​1128/​JVI.​02012-06CrossRefPubMed
72.
go back to reference Wu A, Peng Y, Huang B, Ding X, Wang X, Niu P, Meng J, Zhu Z, Zhang Z, Wang J, Sheng J, Quan L, Xia Z, Tan W, Cheng G, Jiang T (2020) Genome composition and divergence of the novel coronavirus (2019-nCoV) originating in China. Cell Host Microbe 27(3):325–328PubMedPubMedCentral Wu A, Peng Y, Huang B, Ding X, Wang X, Niu P, Meng J, Zhu Z, Zhang Z, Wang J, Sheng J, Quan L, Xia Z, Tan W, Cheng G, Jiang T (2020) Genome composition and divergence of the novel coronavirus (2019-nCoV) originating in China. Cell Host Microbe 27(3):325–328PubMedPubMedCentral
77.
go back to reference Yang J (2020) Prevalence of comorbidities in the novel Wuhan coronavirus (COVID-19) infection: a systematic review and meta-analysis. Int J Infect Dis 94:91–95PubMedPubMedCentral Yang J (2020) Prevalence of comorbidities in the novel Wuhan coronavirus (COVID-19) infection: a systematic review and meta-analysis. Int J Infect Dis 94:91–95PubMedPubMedCentral
78.
go back to reference Xiang P, Xu XM, Gao LL, Wang HZ, Xiong HF, Li RH et al. First case of 2019 novel coronavirus disease with encephalitis ChinaXiv, T202003 (2020), p. 00015 Xiang P, Xu XM, Gao LL, Wang HZ, Xiong HF, Li RH et al. First case of 2019 novel coronavirus disease with encephalitis ChinaXiv, T202003 (2020), p. 00015
80.
go back to reference Olender T, Keydar I, Pinto JM, Tatarskyy P, Alkelai A, Chien M-S, Fishilevich S, Restrepo D, Matsunami H, Gilad Y, Lancet D (2016) The human olfactory transcriptome. BMC Genomics 17:619PubMedPubMedCentral Olender T, Keydar I, Pinto JM, Tatarskyy P, Alkelai A, Chien M-S, Fishilevich S, Restrepo D, Matsunami H, Gilad Y, Lancet D (2016) The human olfactory transcriptome. BMC Genomics 17:619PubMedPubMedCentral
81.
go back to reference Kangeswaran N, Demond M, Nagel M (2015) Deep sequencing of the murine olfactory receptor transcriptome. PLoS One 10(1):e0113170 Kangeswaran N, Demond M, Nagel M (2015) Deep sequencing of the murine olfactory receptor transcriptome. PLoS One 10(1):e0113170
82.
go back to reference Saraiva LR, Ibarra-Soria X, Khan M, Omura M, Scialdone A, Mombaerts P, Marioni JC, Logan DW (2015) Hierarchical deconstruction of mouse olfactory sensory neurons: from whole mucosa to single-cell RNA-seq. Sci Rep 5:18178PubMedPubMedCentral Saraiva LR, Ibarra-Soria X, Khan M, Omura M, Scialdone A, Mombaerts P, Marioni JC, Logan DW (2015) Hierarchical deconstruction of mouse olfactory sensory neurons: from whole mucosa to single-cell RNA-seq. Sci Rep 5:18178PubMedPubMedCentral
83.
go back to reference Sepahi A, Kraus A, Casadei E, Johnston CA, Galindo-Villegas J, Kelly C, Garcia-Moreno D, Munoz P, Mulero V, Huertas M, Salinas I (2019) Olfactory sensory neurons mediate ultrarapid antiviral immune responses in a TrkA-dependent manner. Proc Natl Acad Sci U S A 116(25):12428–12436PubMedPubMedCentral Sepahi A, Kraus A, Casadei E, Johnston CA, Galindo-Villegas J, Kelly C, Garcia-Moreno D, Munoz P, Mulero V, Huertas M, Salinas I (2019) Olfactory sensory neurons mediate ultrarapid antiviral immune responses in a TrkA-dependent manner. Proc Natl Acad Sci U S A 116(25):12428–12436PubMedPubMedCentral
84.
go back to reference Baker E, Lui F (2020) Neuroanatomy, vagal nerve nuclei (Nucleus Vagus). In: StatPearls. StatPearls Publishing, Treasure Island (FL) Baker E, Lui F (2020) Neuroanatomy, vagal nerve nuclei (Nucleus Vagus). In: StatPearls. StatPearls Publishing, Treasure Island (FL)
86.
go back to reference Arbour N, Cote G, Lachance C, Tardieu M, Cashman NR, Talbot PJ (1999) Acute and persistent infection of human neural cell lines by human coronavirus OC43. J Virol 73:3338–3350PubMedPubMedCentral Arbour N, Cote G, Lachance C, Tardieu M, Cashman NR, Talbot PJ (1999) Acute and persistent infection of human neural cell lines by human coronavirus OC43. J Virol 73:3338–3350PubMedPubMedCentral
87.
go back to reference Jacomy H, Fragoso G, Almazan G, Mushynski WE, Talbot PJ (2006) Human coronavirus OC43 infection induces chronic encephalitis leading to disabilities in BALB/C mice. Virology 349:335–346PubMedPubMedCentral Jacomy H, Fragoso G, Almazan G, Mushynski WE, Talbot PJ (2006) Human coronavirus OC43 infection induces chronic encephalitis leading to disabilities in BALB/C mice. Virology 349:335–346PubMedPubMedCentral
88.
go back to reference Espinoza JA, Bohmwald K, Cespedes PF, Gomez RS, Riquelme SA, Cortes CM, Valenzuela JA, Sandoval RA, Pancetti FC, Bueno SM, Riedel CA, Kalergis AM (2013a) Impaired learning resulting from respiratory syncytial virus infection. Proc Natl Acad Sci U S A 110:9112–9117PubMedPubMedCentral Espinoza JA, Bohmwald K, Cespedes PF, Gomez RS, Riquelme SA, Cortes CM, Valenzuela JA, Sandoval RA, Pancetti FC, Bueno SM, Riedel CA, Kalergis AM (2013a) Impaired learning resulting from respiratory syncytial virus infection. Proc Natl Acad Sci U S A 110:9112–9117PubMedPubMedCentral
89.
go back to reference Espinoza JA, Bohmwald K, Cespedes PF, Gomez RS, Riquelme SA, Cortes CM, Valenzuela JA, Sandoval RA, Pancetti FC, Bueno SM, Riedel CA, Kalergis AM (2013b) Impaired learning resulting from respiratory syncytial virusinfection. Proc Natl Acad Sci U S A 110:9112–9117PubMedPubMedCentral Espinoza JA, Bohmwald K, Cespedes PF, Gomez RS, Riquelme SA, Cortes CM, Valenzuela JA, Sandoval RA, Pancetti FC, Bueno SM, Riedel CA, Kalergis AM (2013b) Impaired learning resulting from respiratory syncytial virusinfection. Proc Natl Acad Sci U S A 110:9112–9117PubMedPubMedCentral
90.
go back to reference Jurgens HA, Amancherla K, Johnson RW (2012) Influenza infection induces neuroinflammation, alters hippocampal neuron morphology, and impairs cognition in adult mice. J Neurosci 32:3958–3968PubMedPubMedCentral Jurgens HA, Amancherla K, Johnson RW (2012) Influenza infection induces neuroinflammation, alters hippocampal neuron morphology, and impairs cognition in adult mice. J Neurosci 32:3958–3968PubMedPubMedCentral
91.
go back to reference Vasek MJ, Garber C, Dorsey D, Durrant DM, Bollman B, Soung A, Yu J, Perez-Torres C, Frouin A, Wilton DK, Funk K, DeMasters BK, Jiang X, Bowen JR, Mennerick S, Robinson JK, Garbow JR, Tyler KL, Suthar MS, Schmidt RE, Stevens B, Klein RS (2016) A complement-microglial axis drives synapse loss during virus-induced memory impairment. Nature 534:538–543PubMedPubMedCentral Vasek MJ, Garber C, Dorsey D, Durrant DM, Bollman B, Soung A, Yu J, Perez-Torres C, Frouin A, Wilton DK, Funk K, DeMasters BK, Jiang X, Bowen JR, Mennerick S, Robinson JK, Garbow JR, Tyler KL, Suthar MS, Schmidt RE, Stevens B, Klein RS (2016) A complement-microglial axis drives synapse loss during virus-induced memory impairment. Nature 534:538–543PubMedPubMedCentral
93.
go back to reference Mizuguchi M, Yamanouchi H, Ichiyama T, Shiomi M (2007) Acute encephalopathy associated with influenza and other viral infections. Acta Neurol Scand Suppl 186:45–56PubMed Mizuguchi M, Yamanouchi H, Ichiyama T, Shiomi M (2007) Acute encephalopathy associated with influenza and other viral infections. Acta Neurol Scand Suppl 186:45–56PubMed
94.
go back to reference Elkind MS (2007) Why now? Moving from stroke risk factors to stroke triggers. Curr Opin Neurol 20(1):51–57PubMed Elkind MS (2007) Why now? Moving from stroke risk factors to stroke triggers. Curr Opin Neurol 20(1):51–57PubMed
95.
go back to reference Warren-Gash C, Blackburn R, Whitaker H, McMenamin J, Hayward AC (2018) Laboratory-confirmed respiratory infections as triggers for acute myocardial infarction and stroke: a self-controlled case series analysis of national linked datasets from Scotland. Eur Respir J 51(3):1701794. https://doi.org/10.1183/13993003.01794-2017 Warren-Gash C, Blackburn R, Whitaker H, McMenamin J, Hayward AC (2018) Laboratory-confirmed respiratory infections as triggers for acute myocardial infarction and stroke: a self-controlled case series analysis of national linked datasets from Scotland. Eur Respir J 51(3):1701794. https://​doi.​org/​10.​1183/​13993003.​01794-2017
96.
go back to reference Muhammad S, Haasbach E, Kotchourko M, Strigli A, Krenz A, Ridder DA et al (2011) Influenza virus infection aggravates stroke outcome. Stroke 42(3):783–791PubMed Muhammad S, Haasbach E, Kotchourko M, Strigli A, Krenz A, Ridder DA et al (2011) Influenza virus infection aggravates stroke outcome. Stroke 42(3):783–791PubMed
97.
go back to reference Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ (2020) COVID-19: consider cytokine storm syndromes and immunosuppression [published online ahead of print, 2020 Mar 16]. Lancet S0140-6736(20):30628 Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ (2020) COVID-19: consider cytokine storm syndromes and immunosuppression [published online ahead of print, 2020 Mar 16]. Lancet S0140-6736(20):30628
98.
go back to reference Zhou F (2020) Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 395(10229):1054–1062PubMedPubMedCentral Zhou F (2020) Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 395(10229):1054–1062PubMedPubMedCentral
99.
go back to reference Guo J (2020) Coronavirus disease 2019 (COVID-19) and cardiovascular disease: a viewpoint on the potential influence of angiotensin-converting enzyme inhibitors/angiotensin receptor blockers on onset and severity of severe acute respiratory syndrome coronavirus 2 infection. J Am Heart Assoc 9(7):e016219PubMedPubMedCentral Guo J (2020) Coronavirus disease 2019 (COVID-19) and cardiovascular disease: a viewpoint on the potential influence of angiotensin-converting enzyme inhibitors/angiotensin receptor blockers on onset and severity of severe acute respiratory syndrome coronavirus 2 infection. J Am Heart Assoc 9(7):e016219PubMedPubMedCentral
100.
go back to reference Padroni M (2020) Guillain-Barre syndrome following COVID-19: new infection, old complication? J Neurol 267:1877–1879PubMed Padroni M (2020) Guillain-Barre syndrome following COVID-19: new infection, old complication? J Neurol 267:1877–1879PubMed
102.
go back to reference Cusick MF, Libbey JE, Fujinami RS (2013) Multiple sclerosis: autoimmunity and viruses. Curr Opin Rheumatol 25:496–501PubMedPubMedCentral Cusick MF, Libbey JE, Fujinami RS (2013) Multiple sclerosis: autoimmunity and viruses. Curr Opin Rheumatol 25:496–501PubMedPubMedCentral
104.
105.
go back to reference Saberi A, Akhondzadeh S, Kazemi S (2018) Infectious agents and different course of multiple sclerosis: a systematic review. Acta Neurol Belg 118:361–377PubMed Saberi A, Akhondzadeh S, Kazemi S (2018) Infectious agents and different course of multiple sclerosis: a systematic review. Acta Neurol Belg 118:361–377PubMed
106.
go back to reference Smatti MK, Cyprian FS, Nasrallah GK, Al Thani AA, Almishal RO, Yassine HM (2019) Viruses and autoimmunity: a review on the potential interaction and molecular mechanisms. Viruses 11:762PubMedCentral Smatti MK, Cyprian FS, Nasrallah GK, Al Thani AA, Almishal RO, Yassine HM (2019) Viruses and autoimmunity: a review on the potential interaction and molecular mechanisms. Viruses 11:762PubMedCentral
107.
go back to reference Tanaka R, Iwasaki Y, Koprowski H (1976) Intracisternal virus-like particles in brain of a multiple sclerosis patient. J Neurol Sci 28(1):121–126PubMedPubMedCentral Tanaka R, Iwasaki Y, Koprowski H (1976) Intracisternal virus-like particles in brain of a multiple sclerosis patient. J Neurol Sci 28(1):121–126PubMedPubMedCentral
108.
go back to reference Salmi A, Ziola B, Hovi T, Reunanen M (1982) Antibodies to coronaviruses OC43 and 229E in multiple sclerosis patients. Neurology. 32:292–295PubMed Salmi A, Ziola B, Hovi T, Reunanen M (1982) Antibodies to coronaviruses OC43 and 229E in multiple sclerosis patients. Neurology. 32:292–295PubMed
109.
go back to reference Murray RS, Brown B, Brian D, Cabirac GF (1992a) Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann Neurol 31:525–533PubMedPubMedCentral Murray RS, Brown B, Brian D, Cabirac GF (1992a) Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann Neurol 31:525–533PubMedPubMedCentral
110.
go back to reference Murray RS, Brown B, Brian D, Cabirac GF (1992b) Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann Neurol 31:525–533PubMedPubMedCentral Murray RS, Brown B, Brian D, Cabirac GF (1992b) Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann Neurol 31:525–533PubMedPubMedCentral
111.
go back to reference Sorensen O, Coulter-Mackie MB, Puchalski S, Dales S (1984) In vivo and in vitro models of demyelinating disease. IX. Progression of JHM virus infection in the central nervous system of the rat during overt and asymptomatic phases. Virology. 137:347–357PubMedPubMedCentral Sorensen O, Coulter-Mackie MB, Puchalski S, Dales S (1984) In vivo and in vitro models of demyelinating disease. IX. Progression of JHM virus infection in the central nervous system of the rat during overt and asymptomatic phases. Virology. 137:347–357PubMedPubMedCentral
112.
go back to reference Cristallo A, Gambaro F, Biamonti G, Ferrante P, Battaglia M, Cereda PM (1997) Human coronavirus polyadenylated RNA sequences in cerebrospinal fluid from multiple sclerosis patients. Microbiologica. 2:105–114 Cristallo A, Gambaro F, Biamonti G, Ferrante P, Battaglia M, Cereda PM (1997) Human coronavirus polyadenylated RNA sequences in cerebrospinal fluid from multiple sclerosis patients. Microbiologica. 2:105–114
114.
go back to reference Weber T, Major EO (1997) Progressive multifocal leukoencephalopathy: molecular biology, pathogenesis and clinical impact. Intervirology. 40:98–111PubMed Weber T, Major EO (1997) Progressive multifocal leukoencephalopathy: molecular biology, pathogenesis and clinical impact. Intervirology. 40:98–111PubMed
115.
go back to reference Sun N, Grzybicki D, Castro F, Murphy S, Perlman S (1995) Activation of astrocytes in the spinal cord of mice chronically infected with a neurotropic coronavirus. Virology. 213:482–493PubMedPubMedCentral Sun N, Grzybicki D, Castro F, Murphy S, Perlman S (1995) Activation of astrocytes in the spinal cord of mice chronically infected with a neurotropic coronavirus. Virology. 213:482–493PubMedPubMedCentral
116.
go back to reference Lane TE, Asensio VC, Yu N, Paoletti AD, Campbell IL, Buchmeier MJ (1998) Dynamic regulation of α- and β-chemokine expression in the central nervous system during mouse hepatitis virus-induced demyelinating disease. J Immunol 160:970–978PubMed Lane TE, Asensio VC, Yu N, Paoletti AD, Campbell IL, Buchmeier MJ (1998) Dynamic regulation of α- and β-chemokine expression in the central nervous system during mouse hepatitis virus-induced demyelinating disease. J Immunol 160:970–978PubMed
117.
go back to reference Rima BK, Duprex WP (2005) Molecular mechanisms of measles virus persistence. Virus Res 111(2):132–147PubMed Rima BK, Duprex WP (2005) Molecular mechanisms of measles virus persistence. Virus Res 111(2):132–147PubMed
118.
go back to reference Roberts MT (2005) AIDS-associated progressive multifocal leukoencephalopathy: current management strategies. CNS Drugs 19(8):671–682PubMed Roberts MT (2005) AIDS-associated progressive multifocal leukoencephalopathy: current management strategies. CNS Drugs 19(8):671–682PubMed
119.
go back to reference Sweet TM, Del Valle L, Khalili K (2002) Molecular biology and immunoregulation of human neurotropic JC virus in CNS. J Cell Physiol 191(3):249–256PubMed Sweet TM, Del Valle L, Khalili K (2002) Molecular biology and immunoregulation of human neurotropic JC virus in CNS. J Cell Physiol 191(3):249–256PubMed
120.
go back to reference Gonzalez-Scarano F, Baltuch G (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22:219–240PubMed Gonzalez-Scarano F, Baltuch G (1999) Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22:219–240PubMed
121.
go back to reference Hovelmeyer N, Hao Z, Kranidioti K, Kassiotis G, Buch T, Frommer F, von Hoch L, Kramer D, Minichiello L, Kollias G, Lassmann H, Waisman A (2005) Apoptosis of oligodendrocytes via Fas and TNF-R1 is a key event in the induction of experimental autoimmune encephalomyelitis. J Immunol 175(9):5875–5884PubMed Hovelmeyer N, Hao Z, Kranidioti K, Kassiotis G, Buch T, Frommer F, von Hoch L, Kramer D, Minichiello L, Kollias G, Lassmann H, Waisman A (2005) Apoptosis of oligodendrocytes via Fas and TNF-R1 is a key event in the induction of experimental autoimmune encephalomyelitis. J Immunol 175(9):5875–5884PubMed
122.
go back to reference McLarnon JG, Michikawa M, Kim SU (1993) Effects of tumor necrosis factor on inward potassium current and cell morphology in cultured human oligodendrocytes. Glia 9(2):120–126PubMed McLarnon JG, Michikawa M, Kim SU (1993) Effects of tumor necrosis factor on inward potassium current and cell morphology in cultured human oligodendrocytes. Glia 9(2):120–126PubMed
123.
go back to reference Miller SD, Vanderlugt CL, Begolka WS, Pao W, Neville KL, Yauch RL, Kim BS (1997) Epitope spreading leads to myelin-specific autoimmune responses in SJL mice chronically infected with Theiler’s virus. J Neuro-Oncol 3(Suppl 1):S62–S65 Miller SD, Vanderlugt CL, Begolka WS, Pao W, Neville KL, Yauch RL, Kim BS (1997) Epitope spreading leads to myelin-specific autoimmune responses in SJL mice chronically infected with Theiler’s virus. J Neuro-Oncol 3(Suppl 1):S62–S65
124.
go back to reference Butler N, Pewe L, Trandem K, Perlman S (2006) Murine encephalitis caused by HCoV-OC43, a human coronavirus with broad species specificity, is partly immune-mediated. Virology 347:410–421PubMedPubMedCentral Butler N, Pewe L, Trandem K, Perlman S (2006) Murine encephalitis caused by HCoV-OC43, a human coronavirus with broad species specificity, is partly immune-mediated. Virology 347:410–421PubMedPubMedCentral
125.
go back to reference Moriguchi T (2020) A first case of meningitis/encephalitis associated with SARS-Coronavirus-2. Int J Infect Dis 94:55–58PubMedPubMedCentral Moriguchi T (2020) A first case of meningitis/encephalitis associated with SARS-Coronavirus-2. Int J Infect Dis 94:55–58PubMedPubMedCentral
128.
go back to reference Sedaghat Z, Karimi N (2020) Guillain Barre syndrome associated with COVID-19 infection: A case report. J Clin Neurosci 76:233–235 Sedaghat Z, Karimi N (2020) Guillain Barre syndrome associated with COVID-19 infection: A case report. J Clin Neurosci 76:233–235
129.
go back to reference Zhao H, Shen D, Zhou H, Liu J, Chen S (2020) Guillain-Barré syndrome associated with SARS-CoV-2 infection: causality or coincidence? Lancet Neurol 19(5):383–384 Zhao H, Shen D, Zhou H, Liu J, Chen S (2020) Guillain-Barré syndrome associated with SARS-CoV-2 infection: causality or coincidence? Lancet Neurol 19(5):383–384
130.
go back to reference Dobbs M (2011) Toxic Encephalopathy. Semin Neurol 31(02):184–193 Dobbs M (2011) Toxic Encephalopathy. Semin Neurol 31(02):184–193
132.
go back to reference Chan JF-W, Yuan S, Kok K-H, To KK-W, Chu H, Yang J, Xing F, Liu J, Yip CC-Y, Poon RW-S, Tsoi H-W, Lo SK-F, Chan K-H, Poon VK-M, Chan W-M, Ip JD, Cai J-P, Cheng VC-C, Chen H, Hui CK-M, Yuen K-Y (2020) A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster. Lancet 395(10223):514–523 Chan JF-W, Yuan S, Kok K-H, To KK-W, Chu H, Yang J, Xing F, Liu J, Yip CC-Y, Poon RW-S, Tsoi H-W, Lo SK-F, Chan K-H, Poon VK-M, Chan W-M, Ip JD, Cai J-P, Cheng VC-C, Chen H, Hui CK-M, Yuen K-Y (2020) A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster. Lancet 395(10223):514–523
133.
go back to reference Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y et al (2020) Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395(10223):497–506 Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y et al (2020) Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395(10223):497–506
134.
go back to reference Zhang G, Hu C, Luo L, Fang F, Chen Y, Li J et al (2020) Clinical features and short-term outcomes of 221 patients with COVID-19 in Wuhan, China. J Clin Virol 104364 Zhang G, Hu C, Luo L, Fang F, Chen Y, Li J et al (2020) Clinical features and short-term outcomes of 221 patients with COVID-19 in Wuhan, China. J Clin Virol 104364
Metadata
Title
Neuroinvasion, neurotropic, and neuroinflammatory events of SARS-CoV-2: understanding the neurological manifestations in COVID-19 patients
Authors
Yassine Yachou
Abdeslem El Idrissi
Vladimir Belapasov
Said Ait Benali
Publication date
01-10-2020
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 10/2020
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-020-04575-3

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